The Butterfly, the Ant and the Oregano

It may be hard to imagine a ménage à trois, satisfactory to all parties, in which one member tries to dislodge another with a toxic gas and a third eats the offspring of the other two. But such an arrangement exists, and one of its members may even be sitting quietly in your kitchen’s spice rack.

The story begins with the Large Blue, a butterfly that lays its eggs on the wild oregano plant. The caterpillar munches on the plant’s flower buds for two weeks and then one night drops to the ground. Most ants forage at noon, but by timing its descent at dusk, the infant caterpillar gets adopted by a red ant known as Myrmica that forages only at day’s end. The caterpillar deceives an ant into thinking it is a stray grub from the ant’s own nest. It does so by adopting the grub’s posture and by exuding a scent that mimics that of the ant’s own species.

Taken underground to the Myrmica nest, the adopted caterpillar doesn’t remain a helpless foundling for long. It starts to acquire influence in the ant society by imitating the little clucking sounds made by the ants’ queen. And having gained high status in the nest, it can fulfill the purpose of its visit: to feast on the ants’ larvae. The ants themselves use their larvae as a food source when times are tough, so for their queenly guest to behave like a cannibal may not strike them as all that abhorrent.

The caterpillar gorges on the ant grubs for 10 months, increasing its weight nearly 50 times until it is time to turn into a pupa and then a butterfly.

The Large Blue’s association with ants has been known for more than a century. Only recently have researchers started to explore how the butterfly pulls off the feat of detecting the underground nests of a single species of ant to which its caterpillars are adapted. (The butterfly, widespread in Europe, seeks out a single species of the Myrmica family of ants, but the particular species varies from one region to another in the Large Blue’s territory.)

Considerable puzzlement ensued when experiments to test the butterfly’s ability to sense the presence of Myrmica came up blank.

“It was a huge mystery that none of the experiments seemed to work,” said Naomi E. Pierce, an expert on butterfly-ant interactions at Harvard University.

A surprising solution has been proposed by researchers led by Dario Patricelli and Emilio Balletto at the University of Turin in Italy and Jeremy A. Thomas of the University of Oxford. They have developed evidence that the oregano plant is the crucial mediator between the ants and the Large Blue butterfly.

To fend off ants and other threats, the oregano plant exudes toxic fumes. But Myrmica ants have evolved the ability to detoxify carvacrol, an insecticide that is the principal ingredient of the oregano’s defense system. The Myrmica ants may not particularly like carvacrol, but they do like living near oregano plants because the potent chemical keeps ant competitors away.

The oregano plants are less pleased when a Myrmica ant colony tunnels beneath them and snips at their roots. They double their output of carvacrol, Dr. Thomas’s group reported last month in Proceedings of the Royal Society B. And this, the scientists propose, is the cue for female Large Blues seeking the right place to lay their eggs. An extra strong whiff of carvacrol signals not only the right food plant for the infant caterpillars but also the fact that beneath this particular plant is a nest of Myrmica ants.

“It’s a very nice idea, a really ambitious study because there are so many components that had to be looked at,” Dr. Pierce said.

Despite the hostile relationships among its members, the Large Blue-oregano-Myrmica system holds advantages for all. The oregano sacrifices more than a dozen of its flower buds to each Large Blue caterpillar, but benefits because the growing caterpillar can wipe out the ants that are irritating its roots. The Myrmica ants may lose a few colonies to Large Blue caterpillars, but this is a small price to pay for the oregano’s protection against their many ant rivals. The Large Blue exploits the oregano-Myrmica association to gain safe underground nurseries for its brood.

Perhaps because of the success of its deceptive methods, the Large Blue lays only 50 eggs, fewer than many other butterflies. But its dependence on single species of Myrmica ties its fate to that of the ants.

Dr. Thomas, an ecologist, was called in when the last few colonies of the Large Blue in England were dwindling toward extinction. He spent four years studying the tiny last colony, painfully watching it ebb from 200 butterflies one year to 64 the next and then to 20.

Only as the Large Blue was racing toward extinction in Britain did he and colleagues come to understand why it was fading. The butterfly needed not just any red ant, as was then believed, but a particular species. And the Myrmica is very sensitive to temperature, needing to bring its brood up to warm soil just below the surface. But the soil gets warm enough only under short, or grazed, turf.

“It gradually became clear that it needed just one red ant species and that the butterfly was disappearing because of changes in land use,” Dr. Thomas said. When English farmers ceased grazing their animals on the poorer soil of hillsides, the grasses grew taller, restricting the Myrmica’s habitat. Rabbits, to some degree, took over the grazing, but the myxomatosis virus that devastated the rabbit populations of Britain spelled the end for the Large Blue.

After analyzing his data, Dr. Thomas felt he understood the reason for the butterfly’s decline and could restore it by keeping the turf short in its habitats. “To persuade people to change the management of nature reserves, and then to see the results, took many years,” he said. “By the time I had got people to turn things around, the butterfly was gone.”

To test his ideas, he introduced a nearly identical variety of Large Blue from Sweden. Purists objected that it wasn’t the same as the lost British butterfly. But the British Large Blues varied considerably from one habitat to the next, and the Swedish ones “were very similar to the old British races,” Dr. Thomas said. The Large Blue is now back and flourishing at some 30 sites in Britain.

The Large Blue belongs to an extensive family of butterflies known as lycaenids, which originated some 75 million to 80 million years ago. The first lycaenids most likely had a close relationship with ants, one in which caterpillars secreted foods attractive to ants and were in turn protected by them, Dr. Pierce said. Most lycaenids today retain some kind of relationship with ants. Several species, including the Large Blue, have independently evolved the ability to twist the usual food-defense relationship into a predatory association with their protectors.